Hydraulic signaling in plants

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Hydraulic signals in plants are detected as changes in the organism's water potential that are caused by environmental stress like drought or wounding. [1] The cohesion and tension properties of water allow for these water potential changes to be transmitted throughout the plant.

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Plants respond to external stimuli through thigmomorphogenesis. For example, bending a shoot can cause arrestment of growth on another area of the plant. These types of nonlocal responses can be induced by long distance signaling. Long distance communication in plants must satisfy two things: First, signaling must occur rapidly to an apical area of the plant; Second, the signal must be perceived at the apical site and be converted to a physiological or thigmorphogenetic response. One form of long distance signaling is through hydraulic pulses from the roots to the shoots of a plant. [2] Tree branches and stems contain microchannels that make up the xylem network and serve to carry water longitudinally. Stimuli like wounding can cause tension and compression of plant tissues, which pinches the cross section of the shoot. Hydraulic signaling begins with a local response like water expulsion, creating a suction in the vascular system. The compression of the cross section will then lead to a general increase of hydraulic pressure in the channels of the shoot. [2] This extensive change in hydraulic pressure will lead to activation of hydraulic sensors.

Water potential

The driving force of the movement of water is the water potential gradient. The water potential gradient is defined by comparing the potential energy of water to pure water at standard conditions. This water potential gradient must be maintained from the soil through the plant and into the air via transpiration. [1] In the xylem, water is transported throughout the plant following increasing water potential differences. These differences are determined by soil water availability and vapor pressure deficit. [3]   If this gradient is flipped the translocation of water will occur in the opposite direction. The water potential is the combination of the pressure potential, the osmotic potential and the gravitational contribution.  The translocation of water can be restricted by resistances like stomatal aperture, xylem structure related resistance to flow etc. [1]

Long-distance signaling

In order for plants to respond and adapt to external stimuli, long distance signaling is required. [4] In general terms, long distance signaling is defined as the ability to have a widespread response when just one distinct area is stimulated. [4]   In plants, water uptake must be tightly controlled, so long-distance signaling by hydraulic cues coordinate plants above and below-ground organs. [1]   The daily physiological behavior of plants is tightly controlled by hydraulic signals. [3]   Gradients of water potentials are transferred across the plant through hydraulic signals. If the hydraulic signal originated in the root, it will result in local water potential changes, and consequently turgor changes. The water potential changes can be due to dry soil,  water loss via transpiration or physically wounding the plant.  These local water potential changes are then transmitted quickly over long-distances as hydraulic signals. Hydraulic signaling is fast and effective because of the cohesion and tension properties of water. [1] Hydraulic signals can be propagated downward or upward, relaying water potential gradients throughout the entire plant.

Hydraulic signals can be sensed in a few ways all relating to how an increase in water potential affects the plants.  Because water leaves the cell, there is a reduction in the pressure potential and an increase in solute concentration.  This is one way the hydraulic signal can be sensed, through sensing the osmotic environment.  Increase in water potential also causes mechanical forces on the cell wall and plasma membrane of the cell.  This is the second way to sense hydraulic signaling, by sensing the changes in the mechanical forces on the cell wall. [1]

Experimental methods for studying hydraulic signaling

Linear beam theory

Biomimetic systems can be used to mimic the microchannels inside branches. [2] These synthetic plant systems are made from polydimethylsiloxane (PDMS) and 3D molded like branches and filled with a silicone oil (with viscosity 1 Pa*s). Channels are connected by a differential pressure sensor. The initial branch is straight and the internal water pressure is equal to the atmospheric pressure |Pref-P0=0|. Hydraulic pulses are then induced by automated linear motor deplacement, creating a bend in the synthetic branches which results in a rise in overpressure (Pref), reaching a value of |Pref-P0| or deltaP. Returning back to the initial state of the branch will bring the value of deltaP back to 0. The observation is that overpressure increases quadratically with bending strain. This response changes with variation in beam rigidity.

Nonlinear poroelastic coupling

In a nonlinear poroelastic system, elastic tubes begin straight. When bent, elastic strain increases proportionally with the distance from the initial position. This induces a bending elastic energy per unit of volume that is quadratically related to the transverse radius. The system will lower this elastic energy by squeezing its cross section. This transverse compression leads to a decrease in the channel volume creating a global increase in pressure. Therefore, the mechanism of generating hydraulic pressure is due to the coupling of bending and the transverse deformation of the elastic beam. [2]

Hydraulic signaling in natural branches

Louf et al. has conducted research on hydraulic signaling in 3 species: P. sylvestris, Quercus ilex, and P.alba. Their findings can be summarized by these points: Bending of a branch leads to an increase in xylem water pressure. The magnitude of response depends on the species of plant and the environmental conditions. Hydraulic pulses were found to be greater in trees grown outside with stiffer properties, also proving that elasticity plays a role in hydraulic pulses. [2]

Mechanism

The overall pathway of hydraulic signaling in plants is similar to that of a sensory pathway, starting with basic perception of the signal by a sensor, which then converts the hydraulic signal into a chemical signal: abscisic acid or ABA. [1] This conversion to a chemical signal leads to the control of different physiological responses in the plant since ABA is a plant hormone known to mediate many plant developmental processes including organ size, stomatal closure, and dormancy in the plants’ seeds and buds. [5]

Hydraulic signals are primarily detected as decreases in water potential, [1] usually caused by increases in solute concentration or drought. This decrease in water potential is systemic and transferred throughout the plant vascular network via the xylem. Water follows down the water potential gradient from parenchyma cells into the xylem, ultimately leading to a decrease in pressure potential and osmotic potential in the adjacent cells to the xylem.  The hydraulic sensor, which is yet to be known, resides on the inner membrane of the parenchyma cells and detects the decreases in pressure and solute potential through an unknown mechanism. After detection, the unidentified sensor initiates a signal cascade, leading to a calcium transient and subsequent reactive oxygen species (ROS) formation. These ROS are proposed to go on to target ABA biosynthesis enzymes, leading to synthesis of ABA in the parenchyma and later export to regions of the plant requiring the appropriate responses. In an example, ABA response to a hydraulic signal from the roots- a decrease in water potential- is thought to reach the guard cells to stimulate stomatal closure. Despite an unidentified hydraulic sensor(s) and the mechanism of which this sensor detects decreases in pressure and solute potential in the parenchyma, this primary site of ABA biosynthesis is thought to additionally participate as the main location of hydraulic signal perception, vital to mediation of water potential in the plant. [1]

ABA

Abscisic acid (ABA) is a phytohormone that plays a significant role in the plants’ response to drought conditions. During drought, its biosynthesis is triggered and controls many physiological responses.  ABA triggers root growth at low concentrations and closes stomata to prevent water loss from transpiration. ABA is essential for hydraulic signals because of its response to local water potential changes.  ABA is also known to increase hydraulic conductance by increasing aquaporin expression. [1]

Hydraulic sensors

Although sensor(s) for hydraulic signals are unknown and still being investigated, several sensor candidates have been suggested. One candidate for a hydraulic signal sensor has been MCA1, [6] a plasma membrane protein correlated with mechanosensing via calcium-mediated influx in Arabidopsis thaliana. Research has found that MCA1 increased cytoplasmic calcium concentrations in response to a mechanosensory input: plasma membrane distortion in Arabidopsis.

Another sensor candidate proposed are PERKs, [7] members of the proline-rich receptor kinase family in Arabidopsis as well. PERK4 specifically plays a crucial role in abscisic acid (ABA) signalling and response and has shown to be an ABA- and calcium-activated protein kinase. Both MCA1 and PERK4 appear to correlate with cytoplasmic calcium gradients and an early response to hydraulic signals since calcium is known to be involved in plants’ early responses to mechanosensation. [1]

Despite research on these sensor candidates, both ABA and calcium gradient participation in early events of hydraulic signaling have made it particularly difficult to distinguish the order of which each part plays in the hydraulic signaling pathway. [1]

MCA1

MCA1 has been identified as a candidate for a Ca2+ permeable mechanosensitive channel in Arabidopsis thaliana. [1] Overexpression of plasma membrane protein MCA1 causes an increase in calcium uptake from the roots, which then causes an increase in free calcium in the cytoplasm. MCA1 expression in yeast mutants lacking a high affinity calcium influx system will also increase calcium uptake. [8]

MCA2

MCA2 is a paralog of MCA1 that was identified in Arabidopsis thaliana. Protein sequencing technology reveals that the two genes are 72.7% identical and 89.4% similar in amino acid sequence, making MCA2 a reasonable gene to use in studies to determine the function of MCA1 in calcium uptake. Reverse transcription PCR analysis indicates that MCA2 is expressed in the plasma membrane in leaves, flowers, roots, and stems. Knockout of the MCA2 gene causes a decrease in calcium uptake in the roots, relative to the wildtype, suggesting that the MCA2 gene is involved in calcium uptake. [8]

Using GUS staining, researchers were able to find expressions of MCA1 and MCA2 in the pericycle and endodermis of the root in Arabidopsis. No expression was identified in the cortex or epidermis. Rise in cytosolic calcium levels in the pericycle and endodermis under drought conditions suggest that these cells play a role in calcium signaling. The spatial expression of MCA1 and MCA2 and the changes in calcium concentration in the pericycle and endodermis suggests that both MCA1 and MCA2 play a role in symplastic calcium transport and signaling. [8]

PERK4

Proline-rich extensin-like receptor kinases 4 (PERK4) is a gene expressed in the roots and flowers in Arabidopsis thaliana that localizes in the plasma membrane and plays a role in ABA signaling. [1] Using protein motif analysis, a membrane localization signal, a transmembrane domain, and an intracellular kinase domain were identified in PERK4. To study the role of PERK4 and ABA, mutants were made by inserting T-DNA. PERK4 mutants showed a decrease in ABA sensitivity which affects seedling germination and root tip growth. Mutating PERK4 causes cytosolic free calcium levels to decrease in roots relevant to the wild type. The function of PERK4 has been proposed in early stage ABA signalling to inhibit root elongation by disturbing cytoplasmic calcium gradients. [7]

Ongoing research

Arabidopsis thaliana has been a primary model system in the search for the hydraulic sensor however, has not yet produced a certain answer. [1] Screens for plant mutants affected in hydraulic signaling have been necessary yet, none have been reported so far. [9] Some plant mutants have been distinguished by using the Arabidopsis line pAtH-B6::LUC [10] with lesions upstream of ABA action. [1] Recent years prior to 2013 have shown more hydraulic sensor candidates such as osmosensors and turgor sensors [1] however, research is ongoing as to the specific roles they may play in hydraulic signaling in plants.

Related Research Articles

Abiotic stress is the negative impact of non-living factors on the living organisms in a specific environment. The non-living variable must influence the environment beyond its normal range of variation to adversely affect the population performance or individual physiology of the organism in a significant way.

<span class="mw-page-title-main">Plant hormone</span> Chemical compounds that regulate plant growth and development

Plant hormone are signal molecules, produced within plants, that occur in extremely low concentrations. Plant hormones control all aspects of plant growth and development, from embryogenesis, the regulation of organ size, pathogen defense, stress tolerance and through to reproductive development. Unlike in animals each plant cell is capable of producing hormones. Went and Thimann coined the term "phytohormone" and used it in the title of their 1937 book.

<span class="mw-page-title-main">Abscisic acid</span> Plant hormone

Abscisic acid (ABA) is a plant hormone. ABA functions in many plant developmental processes, including seed and bud dormancy, the control of organ size and stomatal closure. It is especially important for plants in the response to environmental stresses, including drought, soil salinity, cold tolerance, freezing tolerance, heat stress and heavy metal ion tolerance.

<span class="mw-page-title-main">Apoplast</span> Extracellular space, outside the cell membranes of plants

Inside a plant, the apoplast can mean the space outside of cell membranes, where material can diffuse freely; that is, the extracellular spaces. Apoplast can also refer especially to the continuum of cell walls of adjacent cells; fluid and material flows occurring there or in any extacellular space are called apoplastic flow or apoplastic transport.

Water potential is the potential energy of water per unit volume relative to pure water in reference conditions. Water potential quantifies the tendency of water to move from one area to another due to osmosis, gravity, mechanical pressure and matrix effects such as capillary action. The concept of water potential has proved useful in understanding and computing water movement within plants, animals, and soil. Water potential is typically expressed in potential energy per unit volume and very often is represented by the Greek letter ψ.

<span class="mw-page-title-main">Hydrotropism</span>

Hydrotropism is a plant's growth response in which the direction of growth is determined by a stimulus or gradient in water concentration. A common example is a plant root growing in humid air bending toward a higher relative humidity level.

<span class="mw-page-title-main">Tonicity</span> Measure of water potential across a semi-permeable cell membrane

In chemical biology, tonicity is a measure of the effective osmotic pressure gradient; the water potential of two solutions separated by a partially-permeable cell membrane. Tonicity depends on the relative concentration of selective membrane-impermeable solutes across a cell membrane which determine the direction and extent of osmotic flux. It is commonly used when describing the swelling-versus-shrinking response of cells immersed in an external solution.

<span class="mw-page-title-main">Lateral root</span> Plant root

Lateral roots, emerging from the pericycle, extend horizontally from the primary root (radicle) and over time makeup the iconic branching pattern of root systems. They contribute to anchoring the plant securely into the soil, increasing water uptake, and facilitates the extraction of nutrients required for the growth and development of the plant. Lateral roots increase the surface area of a plant's root system and can be found in great abundance in several plant species. In some cases, lateral roots have been found to form symbiotic relationships with rhizobia (bacteria) and mycorrhizae (fungi) found in the soil, to further increase surface area and increase nutrient uptake.

<span class="mw-page-title-main">Guard cell</span> Paired cells that control the stomatal aperture

Guard cells are specialized plant cells in the epidermis of leaves, stems and other organs that are used to control gas exchange. They are produced in pairs with a gap between them that forms a stomatal pore. The stomatal pores are largest when water is freely available and the guard cells turgid, and closed when water availability is critically low and the guard cells become flaccid. Photosynthesis depends on the diffusion of carbon dioxide (CO2) from the air through the stomata into the mesophyll tissues. Oxygen (O2), produced as a byproduct of photosynthesis, exits the plant via the stomata. When the stomata are open, water is lost by evaporation and must be replaced via the transpiration stream, with water taken up by the roots. Plants must balance the amount of CO2 absorbed from the air with the water loss through the stomatal pores, and this is achieved by both active and passive control of guard cell turgor pressure and stomatal pore size.

Drought tolerance is the ability to which a plant maintains its biomass production during arid or drought conditions. Some plants are naturally adapted to dry conditions, surviving with protection mechanisms such as desiccation tolerance, detoxification, or repair of xylem embolism. Other plants, specifically crops like corn, wheat, and rice, have become increasingly tolerant to drought with new varieties created via genetic engineering.

<span class="mw-page-title-main">Phototropism</span> Phototropism is the growth of an plant in response to a light stimulus

Phototropism is the growth of an organism in response to a light stimulus. Phototropism is most often observed in plants, but can also occur in other organisms such as fungi. The cells on the plant that are farthest from the light contain a hormone called auxin that reacts when phototropism occurs. This causes the plant to have elongated cells on the furthest side from the light. Phototropism is one of the many plant tropisms or movements which respond to external stimuli. Growth towards a light source is called positive phototropism, while growth away from light is called negative phototropism. Negative phototropism is not to be confused with skototropism which is defined as the growth towards darkness, whereas negative phototropism can refer to either the growth away from a light source or towards the darkness. Most plant shoots exhibit positive phototropism, and rearrange their chloroplasts in the leaves to maximize photosynthetic energy and promote growth. Some vine shoot tips exhibit negative phototropism, which allows them to grow towards dark, solid objects and climb them. The combination of phototropism and gravitropism allow plants to grow in the correct direction.

Stomatal conductance, usually measured in mmol m−2 s−1 by a porometer, estimates the rate of gas exchange and transpiration through the leaf stomata as determined by the degree of stomatal aperture.

A variation potential (VP) is a hydraulically propagating electrical signal occurring exclusively in plant cells. It is one of three propagating signals in plants, the other two being action potential (AP) and wound potential (WP). Variation potentials are responsible for the induction of many physiological processes and are a mechanism for plant systematic responses to local wounding. They induce changes in gene expression; the production of abscisic acid, jasmonic acid, and ethylene; temporary decreases in photosynthesis; and increases in respiration. Variation potentials have been widely shown in vascular plants.

Plants can be exposed to many stress factors such as disease, temperature changes, herbivory, injury and more. Therefore, in order to respond or be ready for any kind of physiological state, they need to develop some sort of system for their survival in the moment and/or for the future. Plant communication encompasses communication using volatile organic compounds, electrical signaling, and common mycorrhizal networks between plants and a host of other organisms such as soil microbes, other plants, animals, insects, and fungi. Plants communicate through a host of volatile organic compounds (VOCs) that can be separated into four broad categories, each the product of distinct chemical pathways: fatty acid derivatives, phenylpropanoids/benzenoids, amino acid derivatives, and terpenoids. Due to the physical/chemical constraints most VOCs are of low molecular mass, are hydrophobic, and have high vapor pressures. The responses of organisms to plant emitted VOCs varies from attracting the predator of a specific herbivore to reduce mechanical damage inflicted on the plant to the induction of chemical defenses of a neighboring plant before it is being attacked. In addition, the host of VOCs emitted varies from plant to plant, where for example, the Venus Fly Trap can emit VOCs to specifically target and attract starved prey. While these VOCs typically lead to increased resistance to herbivory in neighboring plants, there is no clear benefit to the emitting plant in helping nearby plants. As such, whether neighboring plants have evolved the capability to "eavesdrop" or whether there is an unknown tradeoff occurring is subject to much scientific debate. As related to the aspect of meaning-making, the field is also identified as phytosemiotics.

<span class="mw-page-title-main">High Affinity K+ transporter HAK5</span>

High Affinity K+ transporter HAK5 is a transport protein found on the cell surface membrane of plants under conditions of potassium deprivation. It is believed to act as a symporter for protons and the potassium ion, K+. Firstly discovered in barley, receiving the name of HvHAK1, it was soon after identified in the model plant Arabidopsis thaliana and named HAK5. These transporters belongs to the subgroup I of the KT-HAK-KUP family of plant proteins with obvious homology with both bacterial and fungal transport systems, which experienced a major diversification following land conquest. KT-HAK-KUP transporters are one of four different types of K+ transporter within the cell, but are unique as they do not have a putative pore forming domain like the other three; Shaker channels, KCO channels, HKT transporters. It is activated when the plant is situated in low soil with low potassium concentration, and has been shown to be located in higher concentration in the epidermis and vasculature of K+ deprived plants. By turning on, it increases the plants affinity (uptake) of potassium. Potassium plays a vital role in the plants growth, reproduction, immunity, ion homeostasis, and osmosis, which ensures the plants survival. It is the highest cationic molecule within the plant, accounting for 10% of the plants dry weight, which makes its uptake into the plant important. Each plant species has its own HAK5 transporter that is specific to that species and has different levels of affinity to K+. To operate and activate the HAK5 transporter, the external concentration of K+ must be lower than 10μM and up to 200μM. In Arabidopsis plants, when external potassium concentration is lower than 10μM, it is only HAK5 that is involved with the uptake of K+, then between 10 and 200μM both HAK5 and AKT1 are involved with the uptake of K+. HAK5 is coupled with CBL9/CIPK23 kinase's although the mechanism behind this has not yet been understood.

Feronia, also known as FER or protein Sirene, is a recognition receptor kinase found in plants. FER plays a significant part in the plant immune system as a receptor kinase which assists in immune signaling within plants, plant growth, and plant reproduction. FER is regulated by the Rapid Alkalinization Factor (RALF). FER regulates growth in normal environments but it is most beneficial in stressful environments as it helps to initiate immune signaling. FER can also play a role in reproduction in plants by participating in the communication between the female and male cells. FER is found in and can be studied in the organism Arabidopsis thaliana.

A cytokinin signaling and response regulator protein is a plant protein that is involved in a two step cytokinin signaling and response regulation pathway.

The P-type plasma membrane H+
-ATPase
is found in plants and fungi. For the gastric H+
/K+
ATPase, see Hydrogen potassium ATPase.

As a model organism, the Arabidopsis thaliana response to salinity is studied to aid understanding of other more economically important crops.

Calcium signaling in <i>Arabidopsis</i>

Calcium signaling in Arabidopsis is a calcium mediated signalling pathway that Arabidopsis plants use in order to respond to a stimuli. In this pathway, Ca2+ works as a long range communication ion, allowing for rapid communication throughout the plant. Systemic changes in metabolites such as glucose and sucrose takes a few minutes after the stimulus, but gene transcription occurs within seconds. Because hormones, peptides and RNA travel through the vascular system at lower speeds than the plants response to wounds, indicates that Ca2+ must be involved in the rapid signal propagation. Instead of local communication to nearby cells and tissues, Ca2+ uses mass flow within the vascular system to help with rapid transport throughout the plant. Ca2+ moving through the xylem and phloem acts through a “calcium signature” receptor system in cells where they integrate the signal and respond with the activation of defense genes. These calcium signatures encode information about the stimulus allowing the response of the plant to cater towards the type of stimulus.

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